Next Article in Journal
Magnetic Solid-phase Extraction with Fe3O4/Molecularly Imprinted Polymers Modified by Deep Eutectic Solvents and Ionic Liquids for the Rapid Purification of Alkaloid Isomers (Theobromine and Theophylline) from Green Tea
Previous Article in Journal
Novel Sulfamide-Containing Compounds as Selective Carbonic Anhydrase I Inhibitors
Article Menu
Issue 7 (July) cover image

Export Article

Molecules 2017, 22(7), 1050; doi:10.3390/molecules22071050

Article
Myrtaceae Plant Essential Oils and their β-Triketone Components as Insecticides against Drosophila suzukii
1
Institute of Agriculture and Life Science, Gyeongsang National University, Jinju 52828, Korea
2
Division of Applied Life Science (BK21+ Program), Gyeongsang National University, Jinju 52828, Korea
3
Forest Insect Pests and Diseases Division, National Institute of Forest Science, Seoul 02455, Korea
Present address: R&D Bio Team, Agrigento Co., Ltd, Geochang, Gyeongsangnamdo 50119, Korea
*
Author to whom correspondence should be addressed.
Received: 3 June 2017 / Accepted: 20 June 2017 / Published: 24 June 2017

Abstract

:
Spotted wing drosophila (SWD, Drosophila suzukii (Matsumura), Diptera: Drosophilidae) is recognized as an economically important pest in North America and Europe as well as in Asia. Assessments were made for fumigant and contact toxicities of six Myrtaceae plant essential oils (EOs) and their components to find new alternative types of insecticides active against SWD. Among the EOs tested, Leptospermum citratum EO, consisting mainly of geranial and neral, exhibited effective fumigant activity. Median lethal dose (LD50; mg/L) values of L. citratum were 2.39 and 3.24 for males and females, respectively. All tested EOs except Kunzea ambigua EO exhibited effective contact toxicity. LD50 (µg/fly) values for contact toxicity of manuka and kanuka were 0.60 and 0.71, respectively, for males and 1.10 and 1.23, respectively, for females. The LD50 values of the other 3 EOs-L. citratum, allspice and clove bud were 2.11–3.31 and 3.53–5.22 for males and females, respectively. The non-polar fraction of manuka and kanuka did not show significant contact toxicity, whereas the polar and triketone fractions, composed of flavesone, isoleptospermone and leptospermone, exhibited efficient activity with the LD50 values of 0.13–0.37 and 0.22–0.57 µg/fly for males and females, respectively. Our results indicate that Myrtaceae plant EOs and their triketone components can be used as alternatives to conventional insecticides.
Keywords:
spotted wing drosophila; manuka; kanuka; triketones

1. Introduction

The spotted wing drosophila (SWD, Drosophila suzukii (Matsumura), Diptera: Drosophilidae), is indigenous to South-eastern Asia. It has invaded and spread across North America and Europe and most recently, has been found in South America [1,2,3]. Unlike other closely related Drosophila species, SWD can lay eggs with a serrated ovipositor on maturing and undamaged healthy thin-skinned fruits and inflict substantial economic losses, especially to blueberry, cherry and raspberry [4,5,6]. Developing maggots accelerate fruit softening and decomposition, rendering fruits unmarketable. Current control methods for SWD mainly depend on application of conventional insecticides such as pyrethroids, organophosphates, spinosyns, and neonicotinoids [7,8]. Unfortunately, frequent application of the conventional insecticides is creating public concerns due to their adverse effects on the environment and human health. As a result, there is growing interest in finding less ecologically damaging SWD control methods, such as natural enemies [9] and biopesticides [10,11,12,13], and a strong push to develop new, organic and ecologically sustainable control methods for this destructive pest. Plant essential oils (EOs) could be an eco-friendly alternative to chemical insecticides as they have been reported to have an array of bioactivities, including insecticidal, repellent, and feeding and oviposition deterrent activities for control of a range of insect species [14,15,16]. Other advantages of volatile plant EOs as eco-friendly biopesticides include commercial availability, low cost, multiple modes of action, low toxicity to vertebrates, and brief persistence in the soil [17,18,19,20,21]. The insecticidal activity of EOs against SWD has been investigated [10,11,12,13]. In this study, we assessed the insecticidal activity of Myrtaceae plant EOs and their component β-triketones against adult SWD to find new types of alternatives to current insecticides. Myrtaceae plant EOs were selected because they are known to have insecticidal and repellent activities [10,22,23] and, thus, were assumed to have effective insecticidal activity against SWD.

2. Results

2.1. Chemical Analyses of Active EOs

The chemical composition of a fumigant-active EO, Leptospermum citratum, and two contact toxicity active EOs, L. ericoides (kanuka), and L. scoparium (manuka), are shown in Table 1. Similar to the previous reports [24,25], geranial (33.4%), citronellal (22.8%) and neral (17.8%) were identified as the major components of L. citratum EO.
In contrast, kanuka and manuka EOs consisted of mainly sesquiterpenes (38.5% and 52.0%, respectively) and triketones (27.6% and 34.4%, respectively) and the results were in line with the previous report [27]. The triketones in both kanuka and manuka EOs consisted of flavesone (1), isoleptospermone (2) and leptospermone (3).

2.2. Fumigant Activity of EOs and their Major Components

Among the six tested EOs, only one EO from L. citratum showed 98.0% and 94.0% mortality at a concentration of 11.76 mg/L air against males and females, respectively. In contrast, others showed 0–30.0% and 4.0–16.0% mortality at the same concentration. Median lethal concentration (LC50) values of L. citratum EO were estimated at 2.39 and 3.24 mg/L air against males and females, respectively (Table 2). The LC50 values of the major components geranial, citronellal and neral have been previously reported [10]; therefore, we did not test the fumigant activities of each component individually.

2.3. Contact Toxicity of EOs and Their Major Components

At a concentration of 20 µg/fly, all the tested EOs showed 93–100% male mortality and 98–100% female mortality, with the exception of Kunzea ambigua (61.2%). Kanuka and manuka EOs exhibited 97.9–100% contact toxicity against males and 100% against females at a concentration of 2.5 µg/fly, whereas other EOs showed contact toxicity rates of 14.9–55.3% and 9.9–19.6% against males and females, respectively, at the same concentration. Among the tested EOs, the median lethal dose (LD50) values of kanuka and manuka EOs against males and females were the lowest. The LD50 value of kanuka EO was estimated at 0.71 and 1.23 µg/fly against males and females, respectively, and the LD50 of manuka EO was 0.60 and 1.10 µg/fly, respectively (Table 3). Clover oil and allspice EOs had the next highest levels of toxicity. K. ambigua EO showed the lowest contact toxicity in terms of LD50 value.
Silica gel chromatography of kanuka and manuka EOs gave good separation into a non-polar fraction consisting mainly of sesquiterpene hydrocarbons and a polar fraction that consisted largely of triketones. Further fractionation of polar fraction showed that triketones composed 97.1% of the triketone fraction.
The non-polar fraction of kanuka and manuka EOs did not show significant insecticidal activity, whereas the polar and triketone fractions exhibited significantly higher activity than whole oils (Table 3 and Table 4). The triketone fraction also exhibited higher activity than that of polar fraction in terms of LD50 value (Table 4).

3. Discussion

Leptospermum citratum showed fumigant activity and contact toxicity against adult SWD. Eucalyptus oils have been reported to have insecticidal activity [28]. Among the eucalyptus oils, Melaleuca teretifolia EO, which is composed mainly of geranial and neral, exhibited fumigant and contact toxicity against adult SWD [10]. LC50 and LD50 values of L. citratum for fumigant and contact toxicity, respectively, were similar to those of M. teretifolia. The composition of L. citratum was also similar to M. teretifolia. Therefore, it can be concluded that the toxicity of these EOs may come from geranial and neral.
In contact toxicity tests, the EOs were relatively effective, except for Kunzea ambigua EO. In terms of LD50 values, allspice and clove bud showed similar activity to the previously reported active EOs [10,11,12]. The EOs from allspice and clove bud were reported to consist of thymol [29,30] and eugenol [31], respectively. Thymol is known to have contact toxicity against SWD with an LD50 value of 1.73 µg/fly [11]. Although the contact toxicity of eugenol against SWD was not tested in this study, contact toxicity of eugenol against insect pests is well known [31,32,33]. Activity of thymol and eugenol may be attributed to the contact toxicity of allspice and clove bud, respectively.
Kanuka and manuka EOs were the most active EOs in contact toxicity against SWD compared to previously reported ones [10,11,12,34]. The lack of activity in the non-polar fraction of kanuka and manuka EOs, which contained the hydrocarbons monoterpene and sesquiterpene, clearly showed that the activity is associated with the polar components of oils. The activity of the triketone fraction indicated that the toxicity is related to the presence of triketones, flavesone (1), isoleptospermone (2) and leptospermone (3). Kanuka and manuka EOs and their triketone components are reported to have antimicrobial [27,35], antiviral [36], and acaricidal activities [37,38]. To the best of our knowledge, this is the first report describing the insecticidal activity of β-triketones isolated from kanuka and manuka EOs. Leptospermone, a β-triketone, is a natural product used as an herbicide [39] and inhibits p-hydroxyphenylpyruvate dioxygenase, an enzyme involved in plastoquinone synthesis, as a molecular target site [40]. It is not clear whether the contact toxicity caused by β-triketones is associated with the same mode of action as occurs in the plant; this was not addressed extensively in our study. The β-triketones responsible for contact toxicity against SWD possess multiple carbonyl groups on a six-membered ring (cyclohexane), and this structure is rare in natural phytotoxins. Many derivatives of leptospermone, such as nitisinone and sulcotrione, have been synthesized and selected as herbicides [41]. Some new derivatives of β-triketones with new modes of action, as envisaged by this experiment, are also expected to be used as novel insecticides.
Fumigant activity of dichlorvos and contact toxicity of cypermethrin assessed during these experiments were similar to those previously reported [10,11]. Even though both dichlorvos and cypermethrin are more effective against SWD than the EOs and their components, they have high mammalian toxicity and therefore were expected to have much higher non-target hazards than the EOs and their components.

4. Materials and Methods

4.1. Insects

The colony of SWD was initially obtained from Chonnam National University (Gwangju, Korea) and has been successively maintained in the Insect Chemical Ecology Laboratory, Gyeongsang National University. The colony was maintained in a netted cage (25 × 25 × 20 cm3, BugDorm, Taiwan) with an artificial diet for larvae and 50% sugar solution for adults at 24–26 °C, 60–70% RH and a photoperiod of 16:8 (L:D) [42]. Five- to 7-day-old adults were used for bioassays.

4.2. Chemicals and Fractionation of Essential Oils

Essential oils (EOs) used in this bioassay are listed in Table 5. Six Myrtaceae plant EOs were obtained from Oshadhi Ltd. (Cambridge, England) and La Drome (Die, France). Wakogel C-200 (Wako Pure Chemical, Osaka, Japan) was used for chromatography. Dichlorvos (DDVP), and cypermethrin were purchased from Sigma-Aldrich (St. Louis, MO, USA).
Non-polar and polar fractions of kanuka and manuka EOs were prepared as follows: a sample of oil (5 g) was loaded onto a column of activated silica gel (Wakogel C-200) and eluted with hexane and then with diethyl ether to yield non-polar and polar fractions. The triketone fraction was prepared by further fractionation of the polar fraction with 5% diethyl ether in hexane (Figure 1). The solvent was removed using a rotary evaporator and the fractions were dried and stored at 4 °C before analysis and testing.

4.3. Instrumental Analysis

Gas chromatography (GC) analysis was performed using a GC-17A (Shimadzu, Kyoto, Japan) equipped with a flame ionization detector (FID). A DB-5MS column (30 m × 0.25 mm i.d., 0.25 μm film thickness; J&W Scientific, Folsom, CA, USA) was used for separation of the analytes. GC-mass spectrometry (GC-MS) analysis was performed on a GC-2010 coupled with GCMS-QP2010 plus (Shimadzu) using an HP-Innowax column (30 m × 0.25 mm i.d., 0.25 μm film thickness; J&W Scientific). The oven temperature for GC and GC-MS analyses was programmed as follows: isothermal at 40 °C for 1 min, rose to 250 °C at a rate of 6 °C/min, and was held for 4 min. The injector temperature of GC-FID and GC-MS was 250 °C. The detector temperature of the GC-FID was set at 280 °C. The temperatures of the transfer line and ion source for GC-MS were 250 °C and 230 °C, respectively. One microliter of 5000 ppm EOs dissolved in hexane was injected with a split ratio of 1:50. Each EO was analyzed three times. Helium was used as carrier gas at a flow rate of 1.5 mL/min for GC and of 1.0 mL/min for GC-MS. Most of the components of the EOs were identified by comparing the mass spectra of each peak with those of authentic samples in the NIST/EPA/NIH MS library (Gaithersburg, MD, USA) and by comparison of retention indices determined on two different columns with those of authentic compounds. Flavesone (1), isoleptospermone (2) and leptospermone (3) were identified by comparison of retention indices and mass spectra with previous reports [43,44,45].

4.4. Fumigant Toxicity Assay

For fumigant toxicity assays, a glass cylinder (11 cm in height, 4.5 cm inner diameter; 170 mL, with a sieve placed in the middle) was used. EOs and DDVP dissolved in acetone (20 µL) were applied to a paper disc. After a 10 min incubation to allow the acetone to evaporate, the paper disc was placed on the bottom lid of the cylinder. The concentration range was 0.74–11.76 mg/L. Dichlorvos, an organophosphorus insecticide, was applied as a positive control in range of 0.07–73.5 µg/L. Acetone alone was used as a negative control. Twenty adult SWDs (10 males and 10 females) were placed on the sieve with a cotton wick soaked with 10% sugar solution, thereby preventing their direct contact with the test plant oils and compounds. The top and bottom lids were sealed with Parafilm to prevent fumigant leakage. The insects were maintained at 24–26 °C and 70% relative humidity. After 24 h treatment, they were moved to a new plastic Petri dish (4 cm in height, 9.6 cm diameter) and covered with a lid with a mesh–hole (4 cm diameter) for 10 min. The adult flies were considered dead if their appendages did not move after being touched with a fine brush. All treatments were replicated 5 times.

4.5. Contact Toxicity Assay

To test contact toxicity of EOs and their components, EOs (0.313–20 µg) and three fractions of EOs (0.078–10 µg) dissolved in acetone (1 µL) were topically applied to ventral abdomen using a micro syringe with a repeating dispenser (Hamilton, Reno, NV, USA). As a positive control, cypermethrin, a pyrethroid insecticide, was applied as above at a range of 0.025–50 ng/fly. After application, the adults were placed in a plastic Petri dish (4 cm in height, 9.6 cm diameter) with a cotton wick soaked in 10% sugar solution and covered with a lid which had a mesh-hole (4 cm diameter), thereby preventing fumigant effects of the tested EOs or fractions of EOs. After 24 h treatment, mortality was checked as above. Each treatment was performed 5 times with 20 adult SWDs (10 males and 10 females).

4.6. Statistical Analyses

The corrected mortality was calculated using Abbott’s formula [46]. Probit analysis was used to estimate the LC50 values with dose-response data. Statistical analyses were performed using JMP ver. 9.0.2 (SAS Institute Inc., Cary, NC, USA).

5. Conclusions

Kanuka and manuka EOs and their β-triketone components exhibited excellent contact toxicity against SWD. These are expected to be applied for protection of postharvest fruits. Considering that most insecticides currently in use are synthetic ones, the EOs from Myrtaceae and their components are quite promising and showing potential for the development of natural insecticides. However, further studies addressing the safety of these botanical insecticides to humans and host plants, their formulations, and their modes of action are necessary for practical use of plant EOs and their components as eco-friendly and novel SWD control agents.

Acknowledgments

This research was partially supported by a grant from National Institute of Forest Science, Korea (No. FE0100-1988-01). E.S and M.J were supported by the BK21 plus program, Ministry of Education, Korea. We appreciated to K. Chiluwal (GNU) for editing the manuscript.

Author Contributions

J.K. and C.G.P. designed the experiments. M.J., E.S. and J.K. conducted the experiments. J.K. and C.G.P. wrote the main manuscript. All authors reviewed the manuscript.

Conflicts of Interest

The authors declare no conflict of interest. The founding sponsors had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, and in the decision to publish the results.

References

  1. Asplen, M.K.; Anfora, G.; Biondi, A.; Choi, D.S.; Chu, D.; Daane, K.M.; Gibert, P.; Gutierrez, A.P.; Hoelmer, K.A.; Hutchison, W.D; et al. Invasion biology of spotted wing Drosophila (Drosophila suzukii): A global perspective and future priorities. J. Pest Sci. 2015, 88, 469–494. [Google Scholar] [CrossRef]
  2. Cini, A.; Anfora, G.; Escudero-Colomar, L.A.; Grassi, A.; Santosuosso, U.; Seljak, G.; Papini, A. Tracking the invasion of the alien fruit pest Drosophila suzukii in Europe. J. Pest Sci. 2014, 87, 559–566. [Google Scholar] [CrossRef]
  3. Lasa, R.; Tadeo, E. Invasive drosophilid pests Drosophila suzukii and Zaprionus. indianus (Diptera: Drosophilidae) in Veracruz, Mexico. Fla. Entomol. 2015, 98, 987–988. [Google Scholar] [CrossRef]
  4. Hauser, M. A historic account of the invasion of Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) in the continental United States, with remarks on their identification. Pest Manag. Sci. 2011, 67, 1352–1357. [Google Scholar] [CrossRef] [PubMed]
  5. Goodhue, R.E.; Bolda, M.; Farnsworth, D.; Willams, J.C.; Zalom, F.G. Spotted wing drosophila infestation of California strawberries and raspberries: Economic analysis of potential revenue losses and control. Pest Manag. Sci. 2011, 67, 1396–1402. [Google Scholar] [CrossRef] [PubMed]
  6. Lee, J.C.; Dreves, A.J.; Cave, A.M.; Kawai, S.; Isaacs, R.; Miller, J.C.; Timmeren, S.V.; Bruck, D.J. Infestation of wild and ornamental noncrop fruits by Drosophila suzukii (Diptera: Drosophilidae). Ann. Entomol. Soc. Am. 2015, 108, 117–129. [Google Scholar] [CrossRef]
  7. Bruck, D.J.; Bolda, M.; Tanigoshi, L.; Klick, J.; Kleiber, J.; DeFrancesco, J.; Gerdeman, B.; Spitler, H. Laboratory and field comparisons of insecticides to reduce infestation of Drosophila suzukii in berry crops. Pest Manag. Sci. 2011, 67, 1375–1385. [Google Scholar] [CrossRef] [PubMed]
  8. Van Timmeren, S.; Isaacs, R. Control of spotted wing drosophila, Drosophila suzukii, by specific insecticides and by conventional and organic crop protection programs. Crop. Prot. 2013, 54, 126–133. [Google Scholar] [CrossRef]
  9. Knoll, V.; Ellenbroek, T.; Romeis, J.; Collatz, J. Seasonal and regional presence of hymenopteran parasitoids of Drosophila in Switzerland their ability to parasitize the invasive Drosophila suzukii. Sci. Rep. 2017, 7, 40697. [Google Scholar] [CrossRef] [PubMed]
  10. Jang, M.; Kim, J.; Yoon, K.A.; Lee, S.H.; Park, C.G. Biological activities of Myrtaceae plant essential oils and their major components against Drosophila suzukii (Diptera: Drosophilidae). Pest Manag. Sci. 2017, 73, 404–409. [Google Scholar] [CrossRef] [PubMed]
  11. Park, C.G.; Jang, M.; Yoon, K.A.; Kim, J. Insecticidal and acetylcholinesterase inhibitory activities of Lamiaceae plant essential oils and their major components against Drosophila suzukii (Diptera: Drosophilidae). Ind. Crops Prod. 2016, 89, 507–513. [Google Scholar] [CrossRef]
  12. Kim, J.; Jang, M.; Shin, E.; Kim, J.; Lee, S.H.; Park, C.G. Fumigant and contact toxicity activity of 22 wooden essential oils and their major components against Drosophila suzukii (Diptera: Drosophilidae). Pestic. Biochem. Physiol. 2016, 133, 35–43. [Google Scholar] [CrossRef] [PubMed]
  13. Kim, J.; Jang, M.; Lee, K.T.; Yoon, K.A.; Park, C.G. Insecticidal and enzyme inhibitory activities of sparassol and its analogs against Drosophila suzukii. J. Agric. Food Chem. 2016, 64, 5479–5483. [Google Scholar] [CrossRef] [PubMed]
  14. Isman, M.B. Plant essential oils for pest and disease management. Crop. Prot. 2000, 19, 603–608. [Google Scholar] [CrossRef]
  15. Nerio, L.S.; Olivero-Verbel, J.; Stashenko, E. Repellent activity of essential oils: A review. Bioresour. Technol. 2010, 101, 372–378. [Google Scholar] [CrossRef] [PubMed]
  16. El-Seedi, H.R.; Khalil, N.S.; Azeem, M.; Taher, E.A.; Göransson, U.; Pålsson, K.; Borg-Karlson, A.K. Chemical composition and repellency of essential oils from four medicinal plants against Ixodes ricinus (L.) nymphs (Acari: Ixodidae). J. Med. Entomol. 2012, 49, 1067–1075. [Google Scholar] [CrossRef] [PubMed]
  17. Isman, M.B.; Miresmailli, S.; Machial, C. Commercial opportunities for pesticides based on plant essential oils in agriculture, industry and consumer products. Phytochem. Rev. 2011, 10, 197–204. [Google Scholar] [CrossRef]
  18. Priestley, C.M.; Williamson, E.M.; Wafford, K.A.; Sattelle, D.B. Thymol, a constituent of thyme essential oil, is a positive allosteric modulator of human GABAA receptors and a homo-oligomeric GABA receptor from Drosophila melanogaster. Br. J. Pharmacol. 2003, 140, 1363–1372. [Google Scholar] [CrossRef] [PubMed]
  19. Enan, E. Insecticidal activity of essential oils: Octopaminergic sites of action. Comp. Biochem. Physiol. Part. C: Toxicol. Pharmacol. 2001, 130, 325–337. [Google Scholar] [CrossRef]
  20. Tong, F.; Gross, A.D.; Dolan, M.C.; Coats, J.R. Phenolic monoterpenoid carvacrol inhibits the binding of nicotine to the housefly nicotinic acetylcholine receptor. Pest Manag. Sci. 2013, 69, 775–780. [Google Scholar] [CrossRef] [PubMed]
  21. Tong, F.; Coats, J.R. Quantitative structure–activity relationships of monoterpenoid binding activities to the housefly GABA receptor. Pest Manag. Sci. 2012, 68, 1122–1129. [Google Scholar] [CrossRef] [PubMed]
  22. Renkema, J.M.; Wright, D.; Buitenhuis, R.; Hallett, R.H. Plant essential oils and potassium metabisulfite as repellents for Drosophila suzukii (Diptera: Drosophilidae). Sci. Rep. 2016, 6, 21432. [Google Scholar] [CrossRef] [PubMed]
  23. Park, H.M.; Kim, J.; Chang, K.S.; Kim, B.S.; Yang, Y.J.; Kim, G.H.; Shin, S.C.; Park, I.K. Larvicidal activity of Myrtaceae essential oils and their components against Aedes aegypti, acute toxicity on Daphnia magna, and aqueous residue. J. Med. Entomol. 2011, 48, 405–410. [Google Scholar] [CrossRef] [PubMed]
  24. Lee, Y.S.; Kim, J.; Shin, S.C.; Lee, S.G.; Park, I.K. Antifungal activity of Myrtaceae essential oils and their components against three phytopathogenic fungi. Flavour. Frag. J. 2008, 23, 23–28. [Google Scholar] [CrossRef]
  25. Van Vuuren, S.F.; Docrat, Y.; Kamatou, G.P.P.; Viljoen, A.M. Essential oil composition and antimicrobial interactions of understudied tea tree species. S. Afr. J. Bot. 2014, 92, 7–14. [Google Scholar] [CrossRef]
  26. Van Den Dool, H.; Kratz, P.D. A generalization of the retention index system including linear temperature programmed gas-liquid partition chromatography. J. Chromatogr. A 1963, 11, 463–471. [Google Scholar] [CrossRef]
  27. Porter, N.G.; Wilkins, A.L. Chemical, physical and antimicrobial properties of essential oils of Leptospermum scoparium and Kunzea ericoides. Phytochemistry 1999, 50, 407–415. [Google Scholar] [CrossRef]
  28. Batish, D.R.; Singh, H.P.; Kohli, R.K.; Kaur, S. Eucalyptus essential oil as a natural pesticide. For. Ecol. Manag. 2008, 256, 2166–2174. [Google Scholar] [CrossRef]
  29. Park, I.K.; Kim, J.; Lee, S.G.; Shin, S.C. Nematicidal activity of plant essential oils and components from Ajowan (Trachyspermum. ammi), Allspice (Pimenta dioica) and Litsea (Litsea cubeba) essential oils against pine wood nematode (Bursaphelenchus xylophilus). J. Nematol. 2007, 39, 275–279. [Google Scholar] [PubMed]
  30. Seo, S.M.; Kim, J.; Lee, S.G.; Shin, C.H.; Shin, S.C.; Park, I.K. Fumigant antitermitic activity of plant essential oils and components from ajowan (Trachyspermum ammi), allspice (Pimenta dioica), caraway (Carum carvi), dill (Anethum graveolens), geranium (Pelargonium graveolens), and litsea (Litsea cubeba) oils against Japanese termite (Reticulitermes speratus Kolbe). J. Agric. Food Chem. 2009, 57, 6596–6602. [Google Scholar] [PubMed]
  31. Park, I.K.; Shin, S.C. Fumigant activity of plant essential oils and components from garlic (Allium sativum) and clove bud (Eugenia caryophyllata) oils against the Japanese termite (Reticulitermes speratus Kolbe). J. Agric. Food Chem. 2005, 53, 4388–4392. [Google Scholar] [CrossRef] [PubMed]
  32. Tian, B.L.; Liu, Q.Z.; Liu, Z.L.; Wang, J.W. Insecticidal potential of clove essential oil and its constituents on Cacopsylla chinensis (Hemiptera: Psyllidae) in laboratory and field. J. Econ. Entomol. 2015, 108, 957–961. [Google Scholar] [CrossRef] [PubMed]
  33. Waliwitiya, R.; Isman, M.B.; Verno, R.S.; Riseman, A. Insecticidal activity of selected monoterpenoids and rosemary oil to Agriotes obscurus (Coleoptera: Elateridae). J. Econ. Entomol. 2005, 98, 1560–1565. [Google Scholar] [CrossRef] [PubMed]
  34. Erland, L.A.E.; Rheault, M.R.; Mahmoud, S.S. Insecticidal and oviposition deterrent effects of essential oils and their constituents against the invasive pest Drosophila suzukii (Matsumura) (Diptera: Drosophilidae). Crop. Prot. 2015, 78, 20–26. [Google Scholar] [CrossRef]
  35. Christoph, F.; Kaulfers, P.M.; Stahl-Biskup, E. A comparative study of the in vitro antimicrobial activity of tea tree oils s.l. with special reference to the activity of β-triketones. Planta Med. 2000, 66, 556–560. [Google Scholar] [CrossRef] [PubMed]
  36. Reichling, J.; Koch, C.; Stahl-Biskup, E.; Sojka, C.; Schnitzler, P. Virucidal activity of a β-triketone-rich essential oil of Leptospermum scoparium (Manuka oil) against HSV-1 and HSV-2 in cell culture. Planta Med. 2005, 71, 1123–1127. [Google Scholar] [CrossRef] [PubMed]
  37. Jeong, E.Y.; Kim, M.G.; Lee, H.S. Acaricidal activity of triketone analogues derived from Leptospermum scoparium oil against house-dust and stored-food mites. Pest Manag. Sci. 2009, 65, 327–331. [Google Scholar] [CrossRef] [PubMed]
  38. Fang, F.; Candy, K.; Melloul, E.; Bernigaud, C.; Chai, L.; Darmon, C.; Durand, R.; Botterel, F.; Chosidow, O.; Izri, A.; et al. In vitro activity of ten essential oils against Sarcoptes scabiei. Parasit. Vectors 2016, 9, 594. [Google Scholar] [CrossRef] [PubMed]
  39. Duke, S.O.; Dayan, F.E.; Romagni, J.G.; Rimando, A.M. Natural products as sources of herbicides: current status and future trends. Weed Res. 2000, 40, 99–111. [Google Scholar] [CrossRef]
  40. Dayana, F.E.; Duke, S.O.; Sauldubois, A.; Singh, N.; McCurdy, C.; Cantrella, C. p-Hydroxyphenylpyruvate dioxygenase is a herbicidal target site for β-triketones from Leptospermum scoparium. Phytochemistry 2007, 68, 2004–2014. [Google Scholar] [CrossRef] [PubMed]
  41. Dumas, E.; Giraudo, M.; Goujon, E.; Halma, M.; Knhili, E.; Stauffert, M.; Batisson, I.; Besse-Hoggan, P.; Bohatier, J.; Bouchard, P.; et al. Fate and ecotoxicological impact of new generation herbicides from the triketone family: An overview to assess the environmental risks. J. Hazard. Mater. 2017, 325, 136–156. [Google Scholar] [CrossRef] [PubMed]
  42. Dalton, D.T.; Walton, V.M.; Shearer, P.W.; Walsh, D.B.; Caprile, J.; Isaacs, R. Laboratory survival of Drosophila suzukii under simulated winter conditions of the Pacific Northwest and seasonal field trapping in five primary regions of small and stone fruit production in the United States. Pest Manag. Sci. 2011, 67, 1368–1374. [Google Scholar] [CrossRef] [PubMed]
  43. Van Klink, J.W.; Brophy, J.J.; Perry, N.B.; Weavers, R.T. β-Triketones from Myrtaceae: Isoleptospermone from Leptospermum scoparium and Papuanone from Corymbia dallachiana. J. Nat. Prod. 1999, 62, 487–489. [Google Scholar] [CrossRef] [PubMed]
  44. Perry, N.B.; Van Klink, J.W.; Brennan, N.J.; Harris, W.; Anderson, R.E.; Douglas, M.H.; Smallfield, B.M. Essential oils from New Zealand manuka and kanuka: chemotaxonomy of Kunzea. Phytochemistry 1997, 45, 1605–1612. [Google Scholar] [CrossRef]
  45. Brophy, J.J.; Goldsack, R.J.; Forster, P.I.; Clarkson, J.R.; Fookes, C.J.R. Mass spectra of some β-triketones from australian Myrtaceae. J. Essent. Oil Res. 1996, 8, 465–470. [Google Scholar] [CrossRef]
  46. Abbott, W.S. A method of computing the effectiveness of an insecticide. J. Econ. Entomol. 1925, 18, 265–267. [Google Scholar] [CrossRef]
  • Sample Availability: Samples of the compounds β-triketones are available from the authors.
Figure 1. Gas chromatogram of the triketone fraction and structures of triketones (A) and mass spectra (B–D). 1: flavesone (B); 2: isoleptospermone (C); 3: leptospermone (D).
Figure 1. Gas chromatogram of the triketone fraction and structures of triketones (A) and mass spectra (B–D). 1: flavesone (B); 2: isoleptospermone (C); 3: leptospermone (D).
Molecules 22 01050 g001
Table 1. GC-MS identification, RI values and % peak area contribution of active oil components.
Table 1. GC-MS identification, RI values and % peak area contribution of active oil components.
CompoundRI Values 1L. citratumL. ericoidesL. scoparium
α-Pinene934-19.91.4
β-Pinene9790.1--
Myrcene9890.3-0.4
Limonene1025-1.0-
p-Cymene10270.10.4-
1,8-Cineole1034-1.3-
γ-Terpinene1059-0.6-
Linalool11022.4--
Citronellal115522.8--
Isopulegol11623.2--
Nerol12280.4--
Citronellol123010.7--
Neral124217.8--
Geraniol12532.3--
Geranial127233.4--
Citronellyl acetate13501.1--
α-Cubebene1350-2.14.7
α-Copaene1380-5.05.5
α-Gurjunene1412-0.71.1
β-Caryophyllene1426-1.43.0
6,9-Guaiadiene1444-1.81.8
trans-Muurola-3,5-diene1454-2.07.2
γ-Muurolene1476-2.75.7
α-Selinene1496-4.64.5
γ-Cadinene1523-3.74.9
Calamenene1528-13.913.6
Flavesone1537-8.711.7
α-Copaene-11-ol 1539-0.6-
Isoleptospermone1615-4.95.5
Leptospermone1627-14.017.2
Sum 94.689.388.1
1 RI (retention index) values were calculated following van Den Doold and Kratz on a non-polar column (DB-5MS) [26].
Table 2. LC50 values of fumigant essential oils active against SWD.
Table 2. LC50 values of fumigant essential oils active against SWD.
Essential OilLC50 (mg/L)95% CL (mg/L)Slope ± SEEffect Test
χ2P
Male
Leptospermum citratum2.391.42–3.4404.34 ± 1.2626.84<0.0001
DDVP0.24 × 10−30.04×10−3–0.50 × 10−31.44 ± 0.6020.81<0.0001
Female
Leptospermum citratum3.241.99–4.504.62 ± 1.3728.34<0.0001
DDVP0.36 × 10−30.20 × 10−3–0.66 × 10−31.55 ± 0.9022.38<0.0001
CL: confidence limit.
Table 3. LD50 values of contact toxicity of essential oils against SWD.
Table 3. LD50 values of contact toxicity of essential oils against SWD.
Essential OilLD50 (µg/fly)95% CL (µg/fly)Slope ± SEEffect Test
χ2P
Male
Leptospermum citratum3.311.92–4.931.77 ± 0.5025.19<0.0001
Leptospermum ericoides0.710.35–1.241.52 ± 0.5326.96<0.0001
Leptospermum scoparium0.600.28–1.071.57 ± 0.5924.37<0.0001
Kunzea ambigua7.34na–11.921.28 ± 0.872.310.1287
Pimenta dioica2.261.25–3.612.14 ± 0.7822.24<0.0001
Syzygium aromaticum2.111.04–3.381.85 ± 0.6719.35<0.0001
Cypermethrin0.05 × 10−30.02 × 10−3–0.54 × 10−32.09 ± 0.9420.68<0.0001
Female
Leptospermum citratum5.223.18–7.661.56 ± 0.4323.53<0.0001
Leptospermum ericoides1.230.75–2.171.72 ± 0.5438.70<0.0001
Leptospermum scoparium1.100.60–1.861.37 ± 0.3833.40<0.0001
Kunzea ambigua16.949.07–na1.32 ± 0.832.700.100
Pimenta dioica3.551.88–5.411.39 ± 0.3820.36<0.0001
Syzygium aromaticum3.532.07–5.201.80 ± 0.5025.73<0.0001
Cypermethrin0.06 × 10−30.02 × 10−3–0.12 × 10−31.51 ± 0.5218.64<0.0001
CL: confident limit, na: not available.
Table 4. LD50 values for the non-polar and polar chromatographic fractions of L. ericoides and L. scoparium and the triketone fraction of L. scoparium against SWD.
Table 4. LD50 values for the non-polar and polar chromatographic fractions of L. ericoides and L. scoparium and the triketone fraction of L. scoparium against SWD.
Essential OilLD50 (µg/fly)95% CL (µg/fly)Slope ± SEEffect Test
χ2P
Male
Leptospermum ericoides (NF)24.830.07–na0.33 ± 0.600.310.58
Leptospermum ericoides (PF)0.370.19–0.691.07 ± 0.3127.77<0.0001
Leptospermum scoparium (NF)7.253.07–17.140.89 ± 0.632.130.14
Leptospermum scoparium (PF)0.380.21–0.671.37 ± 0.4132.97<0.0001
Triketone fraction (97.1%)0.130.05–0.241.91 ± 0.8023.42<0.0001
Female
Leptospermum ericoides (NF)86.998.61–na0.48 ± 0.840.340.56
Leptospermum ericoides (PF)0.650.38–1.151.52 ± 0.4538.55<0.0001
Leptospermum scoparium (NF)22.196.23–na0.59 ± 0.690.780.38
Leptospermum scoparium (PF)0.570.34–0.981.75 ± 0.5640.28<0.0001
Triketone fraction (97.1%)0.220.13–0.392.16 ± 0.8234.14<0.0001
CL: confident limit, na: not available, NF: non-polar fraction, PF: polar fraction.
Table 5. List of tested essential oils.
Table 5. List of tested essential oils.
Essential OilScientific NameExtraction PartOriginSource
Leptospermum citratum organicLeptospermum citratum (=L. petersonii)BlossomsAustralia/TasmaniaOshadhi
KanukaLeptospermum ericoides (=Kunzea ericoides)LeavesSouth AfricaOshadhi
ManukaLeptospermum scopariumLeavesNew ZealandOshadhi
KunzeaKunzea ambiguaLeavesAustraliaLa Drome
AllspicePimenta dioicaBerriesJamaicaOshadhi
Clove budSyzygium aromaticumBudMadagascarLa Drome
Molecules EISSN 1420-3049 Published by MDPI AG, Basel, Switzerland RSS E-Mail Table of Contents Alert
Back to Top